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The Electronic Structure of Non-Heme Iron(III)-Hydroperoxo and Iron(III)-Peroxo Model Complexes Studied by Mo1 ssbauer and Electron Paramagnetic Resonance Spectroscopies A. Jalila Simaan,‡ Fre´ de´ ric Banse,‡ Jean-Jacques Girerd,‡ Karl Wieghardt,† and Eckhard Bill*,† Laboratoire de Chimie Inorganique, UMR CNRS 8613, Universite´ Paris-Sud, F-91405 Orsay, France, and Max-Planck-Institut fu¨r Strahlenchemie, D-45470 Mu¨lheim an der Ruhr, Germany
ReceiVed June 18, 2001 Ferric peroxo complexes are currently extensively studied due to their proposed occurrence as reactive intermediates in the catalytic oxygenation reactions of cytochrome P4501 and bleomycin.2 Recently, several mononuclear nonheme Fe(III)hydroperoxo3-7 and Fe(III)-peroxo4b-c,5b,8,9 complexes have been prepared in solution and studied by UV-visible, EPR, Resonance Raman, and Mass Spectrometry.10 The two species displayed in Scheme 1 have been characterized in solution as purple low-spin Fe(III)-hydroperoxo (1) which converts upon addition of base to a blue Fe(III)-η2-peroxo species (2).4 Here, we report a detailed study of these two compounds by EPR and Mo¨ssbauer spectroscopy. Solutions of 1 were prepared from [(trispicMeen)FeCl]Cl‚ 2.5H2O (trispicMeen represents the ligand N-methyl-N,N′,N′-tris(pyridylmethyl)ethane-1,2-diamine). 100-fold excess of hydrogen peroxide was added to a 1.7 mM methanolic solution of the * To whom correspondence should be addressed. E-mail: bill@ mpi-muelheim.mpg.de. ‡ Universite´ Paris-Sud. † Max-Planck-Institut fu¨r Strahlenchemie. (1) (a) Sono, M.; Roach, M. P.; Coulter, E. D.; Dawson, J. H. Chem. ReV. 1996, 96, 2841. (b) Selke, M.; Valentine, J. S. J. Am. Chem. Soc. 1998, 120, 2652. (c) Davydov, R.; MacDonald, I. D. G.; Makris, T. M.; Sligar, S. G.; Hoffman, B. M. J. Am. Chem. Soc. 1999, 121, 10654. (d) Davydov, R.; Yoshida, T.; Ikeda-Saito, M.; Hoffman, B. M. J. Am. Chem. Soc. 1999, 121, 10656. (2) (a) Burger, R. M.; Peisach, J.; Horwitz, S. B. J. Biol. Chem. 1981, 256, 11636. (b) Sam, J. W.; Tang, X.-J.; Peisach, J. J. Am. Chem. Soc. 1994, 116, 5250. (c) Que, L., Jr.; Ho, R. Y. N. Chem. ReV. 1996, 96, 2607. (d) Solomon, E. I.; Brunold, T. C.; Davis, M. I.; Kemsley, J. N.; Lee, S. K.; Lehnert, N.; Neese, F.; Skulan, A. J.; Yang, Y.-S.; Zhou, J. Chem. ReV. 2000, 100, 235. (3) (a) Lubben, M.; Meetsma, A.; Wilkinson, E. C.; Feringa, B.; Que, L. Jr. Angew. Chem., Int. Ed. Engl. 1995, 34, 1512. (b) Kim, C.; Chen, K.; Kim, J.; Que, L., Jr. J. Am. Chem. Soc. 1997, 119, 5964. (c) Ho, R. Y. N.; Roelfes, G.; Feringa, B. L.; Que, L., Jr. J. Am. Chem. Soc. 1999, 121, 264. (d) Roelfes, G.; Lubben, M.; Chen, K.; Ho, R. Y. N.; Meestma, A.; Genseberger, S.; Hermant, R. M.; Hage, R.; Mandal, S. K.; Young, V. G., Jr.; Zang, Y.; Kooijman, H.; Spek, A. L.; Que, L., Jr., Feringa, B. L. Inorg. Chem. 1999, 38, 1929. (4) (a) Mialane, P.; Novorojkine, A.; Pratviel, G.; Aze´ma, L.; Slany, M.; Godde, F.; Simaan, A.; Banse, F.; Kargar-Grisel, T.; Bouchoux, G.; Sainton, J.; Horner, O.; Guilhem, J.; Tchertanov, L.; Meunier, B.; Girerd, J.-J. Inorg. Chem. 1999, 38, 1085-1092. (b) Simaan, A. J.; Banse, F.; Mialane, P.; Kargar-Grisel, T.; Bouchoux, G.; Boussac, A.; Un, S.; Girerd J.-J. Eur. J. Inorg. Chem. 1999, 993-996. (c) Simaan, A. J.; Do¨pner, S.; Banse, F.; Bourcier, S.; Bouchoux, G.; Boussac, A.; Hildebrandt, P.; Girerd, J. J. Eur. J. Inorg. Chem. 2000, 1627. (5) (a) Bernal, I.; Jensen, M.; Jensen, K. B.; MacKenzie, C. J.; Toftlund, H.; Tuchagues, J.-P. J. Chem. Soc., Dalton Trans. 1995, 3667. (b) Jensen, K. B.; McKenzie, C. J.; Nielsen, L. P.; Pedersen, J. Z.; Svendsen, H. M. Chem. Commun. 1999, 1313. (6) De Vries, M. E.; La Crois, R. M.; Roelfes, G.; Kooijman, H.; Spek, A. L.; Hage, R.; Feringa, B. L. Chem. Commun. 1997, 1549. (7) Lippai, I.; Magliozzo, R. S.; Peisach, J. J. Am. Chem. Soc. 1999, 121, 780. (8) (a) Ahmad, S.; McCallum, J. D.; Shiemke, A. K.; Appelman, E. H.; Loehr, T. M.; Sanders-Loehr, J. Inorg. Chem. 1988, 27, 2230. (b) Neese, F.; Solomon, E. I. J. Am. Chem. Soc. 1998, 120, 12829. (9) Ho, R. Y. N.; Roelfes, G.; Hermant, R.; Hage, R.; Feringa, B. L.; Que, L. Jr. Chem. Commun. 1999, 2161. (10) Girerd, J. J.; Banse, F.; Simaan, A. J. Structure and Bonding; SpringerVerlag: New York, 2000; Vol. 97, pp 145-177.
Figure 1. X-band EPR spectrum of the peroxo compound 2 (aliquot of the Mo¨ssbauer sample, 47% enriched with 57Fe). Experimental conditions: temperature 10 K, microwave frequency 9.64405 GHz, modulation 1.28 mT/100 kHz. The solid line is a spin Hamiltonian simulation with parameters D ) -1.7 cm-1, E/D ) 0.08, σ(E/D) ) 0.025, B4 ) -0.004 cm-1, g ) 2, and Gaussian line width Γ ) 60 mT (at g ) 1, frequency dependent part only, isotropic). The arrow marks an additional Gaussian signal of a rhombic Fe(III) high-spin contamination, which was simulated with an isotropic effective g value of 4.27. The inset shows the low-field part of the experimental spectrum with alternative simulations with B4 ) 0 (dashed line).
Scheme 1
ferrous starting complex. Compound 1 was converted to 2 by addition of 5 equiv of Et3N. X-band EPR and Mo¨ssbauer spectra of the 47% 57Fe enriched complexes 1 and 2 were recorded at cryogenic temperatures (below 50 K). The EPR spectrum of 1 displays a characteristic low-spin ferric spectrum (S ) 1/2, g ) 2.12, 2.19, 1.95), as reported previously,4 and an ubiquitous high-spin signal at g ) 4.3 (S ) 5/2 and E/D ) 1/3). In agreement with the corresponding Mo¨ssbauer spectra, it is established that the latter signal amounts to ca. 12% of total iron in our best preparations. It is most probably due to an oxidative deterioration product of 1. Figure 1 shows the X-band EPR spectrum of 2 at 10 K. Prominent derivative signals at g ) 7.4, 5.7, and 4.5 are typical for a high-spin ferric species (S ) 5/2). In addition, an isotropic weak signal at g ) 4.27 is observed and assigned to deterioration products. Additional very weak signals at g ) 2 are due to the presence of residual low-spin complexes. Thus, 2 exhibits a signal of a high-spin Fe(III) ion with almost axial zero-field splitting (ZFS).4b The signals at g ≈ 7.4 and g ≈ 4.5 are assigned to the
10.1021/ic010635e CCC: $20.00 © 2001 American Chemical Society Published on Web 11/14/2001
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Inorganic Chemistry, Vol. 40, No. 26, 2001 6539
effective values g′y(1/2) and g′x(1/2) of the ms ) (1/2 Kramers doublet, respectively. The signal at g ≈ 5.7 corresponds to the effective g′z(3/2) of the middle doublet ms ) (3/2. From the temperature dependence of the relative subspectra intensities (2-15 K), a negative axial ZFS parameter (D < 0) was established with ms ) (1/2 being the excited state. We have successfully simulated the spectrum only by using the somewhat unusual spin Hamiltonian (eq 1).
[
H ) D Sz2 with
]
S(S + 1) E 2 + (Sx - Sy2) + O4 + µBBgS (1) 3 D
O4 ) -2/3B4[O40 + 20 x2 O43] + B40O40
O4 is a phenomenological symmetry adapted fourth order term in the usual effective spin Hamiltonian. The O4m terms represent equivalent operators of fourth degree in S and the parameters B4 and B40 parametrize cubic and trigonal contributions to the ZFS.11 We set B40 to zero and restricted the optimization to values of D, E/D, and B4. The physical effect of the additional ZFS term is a mixing of ms ) (1/2 and (5/2 levels, which introduces a relative shift of the energies and effective g values of these Kramers doublets. In agreement with the Mo¨ssbauer spectra (see below), a satisfactory fit was obtained with D ) -1.7 cm-1, E/D ) 0.08, and B4 ) -0.004 cm-1 (see Figure 1). We note that it has not been possible to reproduce the EPR spectrum without the fourthorder term in eq 1. Indeed, neither the exact position of the different resonances nor their relative intensities could be satisfactorily fitted without this term. With the best value B4 ) -0.004 cm-1, the simulated derivative lines appear at effective g values g′y(1/2) ) 7.43, g′x(1/2) ) 4.53, and g′z(3/2) ) 5.69, in contrast to g′y(1/2) ) 7.74, g′x(1/2) ) 4.22, and g′z(3/2) ) 5.62 for B4 ) 0. The variation shows the influence of B4 on the ms ) (1/2 wavefunctions. A simulation for the latter case is shown in the inset of Figure 1. Moreover, the peculiar differences in line widths of the resonances, particularly g′y(1/2) and g′x(1/2), could be easily simulated by introducing an E/D strain. A Gaussian distribution for the rhombicity parameter was adopted, whereas the intrinsic linewidth was taken to be frequency constant, which leads to a variation of the linewidths in the field swept spectrum according to the respective g values. Using this model the experimental pattern is nicely reproduced with a half width for the E/D distribution of σ(E/D) ) 0.025. Magnetic Mo¨ssbauer spectra of the Fe(III)OOH and Fe(III)O2 species 1 and 2 were measured at liquid helium temperature with applied fields of 0.04, 3, and 7 T. As shown in Figure 2, the spectra of the hydroperoxo complex 1 are rather broad and show only weak overall splitting. This is quite typical for Fe(III) lowspin systems.12 The pattern is superimposed by the widely split six-line spectrum of a minor high-spin ferric component (ca. 12%), which was simulated adopting a rhombic S ) 5/2 species using the EPR parameters from above. The pronounced asymmetry of the low-spin spectra of 1 indicates an anisotropy of the hyperfine tensor in conjunction with a large quadrupole splitting. The small isomer shift, δ, of 0.19 mm s-1 at 4.2 K is typical for an iron(III) low-spin complex.12 The spectra were simulated with the usual spin Hamiltonian approach for S ) 1/2 by using a magnetic hyperfine coupling tensor A/gNβN ) (+7.77, -3.65, -41.09) T, and the anisotropic g values were determined by EPR. The elements of the g matrix were all set to be positive. This is not a constraint since the Mo¨ssbauer spectra are sensitive only for the (11) Abragam, A.; Bleaney, B. Electron Paramagnetic Resonance of Transition Ions; Oxford University Press: Oxford, 1970. (12) Debrunner, P. G. Mo¨ ssbauer Spectroscopy of Iron Porphyrins; Debrunner, P. G., Ed.; VCH: Weinheim, 1989; Vol. III, pp 137-234.
Figure 2. Magnetic Mo¨ssbauer spectra of complex 1 measured at 4.2 K with fields of 0.04, 3, and 7 T applied perpendicular to the γ rays. The solid line is a simulation for the hydroperoxo species “FeOOH” with parameters S ) 1/2, g ) (2.12, 2.19, 1.95), δ ) 0.19 mm s-1, ∆EQ ) -2.01 mm.s-1, η ) 0.4, R ) 43° (Euler angle), and A/gNβN ) (7.77, -3.65, -41.09) T. The dashed line represents a rhombic Fe(III) highspin contamination “X” (S ) 5/2, D ) 1.5 cm-1, E/D ) 0.33, g ) 2, A/gNβN ) -21 T, 12% relative intensity).
products giAi. The electric field gradient (efg) tensor has a large, negative main component, Vzz ) -2.01 mm s-1, and a relatively small asymmetry parameter, η ) 0.4. The fits could be slightly improved by the introduction of an Euler rotation of the efg tensor around the z axis by an angle R ) 43° with respect the principal axes systems of A and g tensors; rotations around the x or y axes were found to be less than 2°, which indicates colinearity of the principal z axes of the three coupling tensor tensors. The Mo¨ssbauer parameters can be qualitatively rationalized in a ligand field description, which strongly implies a low-spin Fe(III) complex with (dxz, dyz)4(dxy)1 electron configuration, in excellent agreement with the previous interpretation of the EPR g values of this complex4c and other models10 of activated Bleomycin.13 The parametrization uses the crystal-field model developed by Griffith14 for the description of the spin-orbit interaction of distorted (t2g)5 complexes. The best solutions for 1 within Taylor’s “proper axes” system (V < 2/3 ∆)15 imposes a relatively large axial splitting to the t2g orbital set, ∆/λ ) -11.4 with a weak rhombic distortion, V/λ ) 4.4c,10 This splitting scheme was interpreted as the result of dominating antibonding interaction of the iron |xy〉 orbital with the π* orbital of the hydroperoxo group (if this is positioned along the y direction).10,13 The resulting anisotropy of the valence electrons caused by the electron hole in a single “pan-cake” shaped dxy orbital is expected to induce a strong negatiVe valence contribution to the main component of the efg in the z direction (and a small asymmetry parameter), in accordance with the experimental observation. The asymmetry of the experimental magnetic hyperfine tensor A is also consistent with the dxy hole picture. The orbital coefficients in this model16 lead to strong orbital and spin-dipolar contributions to A, which explain the large, negative A value in the direction of the efg main component. The best solution for the A tensor that can be obtained in the ligand-field picture (with κ ) 0.35, P (13) Veselov, A.; Sun, H.; Sienkiewicz, A.; Taylor, H.; Burger, R. M.; Scholes, C. P. J. Am. Chem. Soc. 1995, 117, 7508-7512. (14) Griffith, J. S. Proc. R. Soc. London, A 1956, 235, 23-36. (15) Taylor, C. P. S. Biochim. Biophys. Acta 1977, 491, 137-149. (16) Oosterhuis, W. T.; Lang, G. Phys. ReV. 1969, 178, 439-456.
6540 Inorganic Chemistry, Vol. 40, No. 26, 2001
Figure 3. Magnetic Mo¨ssbauer spectra of complex 2 measured at 4.2 with fields of 0.04, 3, and 7 T applied perpendicular to the γ rays. The solid line is a simulation for the peroxo species “FeOO” with parameters S ) 5/2, D ) -1.7 cm-1, E/D ) 0.08, B4 ) -0.004 cm-1, g ) 2, δ ) 0.64 mm s-1, ∆EQ ) +1.37 mm.s-1, η ) 0.98, and A/gNβN ) (-22.71, -22.09, -20.40) T.
) 49.25 T) is A/gNβN ) (+2.3, -6.0, -41.1) T, which is very close to the experimental value. Hence, the magnetic Mo¨ssbauer spectra support the description of 1 as a system with (dxz, dyz)4(dxy)1 electron configuration with a destabilized dxy orbital in the t2g orbital set, which is due to π interaction of with the OOH group. We note that the Griffith model might not be fully valid in its simplest form as it was applied here if the symmetry is less than rhombic. Recently, such a deviation was noted for another low-spin Fe(III) center from a rotation of the g and A tensors, as determined from complementary 57Fe EPR and Mo¨ssbauer data.17 We cannot exclude that such low-symmetry effects are also prevailing in the electronic structure of 1, which is entirely asymmetric. (We gratefully acknowledge a reviewer’s comment pointing out this limitation.) The peroxo complex 2 exhibits a well resolved magnetic hyperfine pattern in the applied-field Mo¨ssbauer spectra, as shown in Figure 3. The large overall splitting indicates the presence of strong internal fields on the order of 54 T, which is typical for high-spin ferric ions.18 The spectra were readily simulated by using the ZFS parameters derived from the EPR simulations. They corroborate particularly the negative sign of the axial ZFS parameter. We mention that a very similar fit could be obtained without the fourth order parameter B4, yielding slightly different (17) Popescu, V. C.; Mu¨nck, E.; Fox, B. G.; Sanakis, Y.; Cummings, J. R.; Turner, I. M.; Nelson, M. J. Biochemistry 2001, 40, 7984-7991. (18) Greenwood, N. N.; Gibb, T. C. Mo¨ ssbauer Spectroscopy; Chapman and Hall Ltd.: London, 1971.
Communications axial and rhombic parameters, D ) -1.1 cm-1 and E/D ) 0.08. For consistency, however, the same model parameters were applied as used in the EPR simulations. The other Mo¨ssbauer parameters obtained are: i) the large isomer shift δ ) 0.64 mm s-1, ii) the large quadrupole splitting ∆EQ ) +1.37 mm s-1 with maximal asymmetry η ) 0.98, and iii) the slightly anisotropic magnetic hyperfine tensor A/gNβN ) (-22.71, -22.09, -20.40) T. The isomer shift and quadrupole splitting of compound 2 are both unusually large for typical high-spin ferric complexes,18 but interestingly, they closely resemble those of the peroxo-diferric intermediate of methane monooxygenase19 and those of a synthetic (µ-1,2-peroxo)diiiron(III) compound (δ ) 0.66 mm s-1, ∆EQ ) 1.40 mm s-1).20 A previous Mo¨ssbauer and EPR investigation of a peroxoferriporphyrin complex21 also revealed similar properties for the FeOO unit in a heme environment. Particularly, the isomer shift and magnetic hyperfine coupling constants are large and very close to those of 2, whereas the quadrupole splitting is significantly lower (+0.62 mm s-1). It is interesting to note that similarly high values of δ are otherwise observed only for the Fe(III) highspin site of nitrosylated nonheme compounds with {FeNO}7 centers.22,23 The large isotropic part of the magnetic hyperfine tensor (A/gNβN ) -21.7 T) is also in the upper range of typical values found for ionic ferric systems (-20 to -22 T).24 Thus, the Mo¨ssbauer parameters reveal the presence of a high-spin Fe(III) moiety with relatively low total covalent delocalization of valence electrons. The unusally large quadrupole splitting for a 3d (t2g)3(eg)2 configuration resembles those of µ-oxo-diiron(III) complexes. The origin of those values was assigned to prevailing anisotropy of the 3d population due to anisotropic covalency, as it is induced by a single short oxo bond.25 MO calculations on [Fe(EDTA)(O2)]-3 support the spectroscopically deduced side-on binding mode of the peroxo ligand.8b From this model study, a dominating strong, covalent σ bond between Fe dxy and peroxide π was identified, which provides a perfect explanation for the large efg and the anisotropy of the A tensor for the peroxo complex 2. Supporting Information Available: Experimental Section. This material is available free of charge via the Internet at http://pubs.acs.org.
IC010635E (19) (a) Liu, K. E.; Valentine, A. M.; Wang, D.; Huynh, G. H.; Edmonson, D. E.; Salifoglou, A.; Lippard, S. J. J. Am. Chem. Soc. 1995, 117, 10174. (b) Liu, K. E.; Valentine, A. M.; Qiu, D.; Edmonson, D. E.; Appelman, E. H.; Spiro, T. G.; Lippard, S. J. J. Am. Chem. Soc. 1995, 117, 4997. (20) Kim, K.; Lippard, S. J. J. Am. Chem. Soc. 1996, 118, 4914. (21) Burstyn, J. N.; Roe, J. A.; Miksztal, A. R.; Shaevitz, B. A.; Lang, G.; Valentine, J. S. J. Am. Chem. Soc. 1988, 110, 1382-1388. (22) Rodriguez, J. H.; Xia, Y.-M.; Debrunner, P. G. J. Am. Chem. Soc. 1999, 121, 7846-7863. (23) Hauser, C.; Glaser, T.; Bill, E.; Weyhermu¨ller, T.; Wieghardt, K. J. Am. Chem. Soc. 2000, 122, 4352-4365. (24) Srivastava, J. K.; Bhargara, S. C.; Iyengar, P. K.; Thosar, B. V. In AdVances in Mo¨ ssbauer Spectroscopy; Thosar, B. V., Iyengar, P. K., Eds.; Elsevier: New York, 1983; pp 1-121. (25) Rodriguez, J. H.; Xia, Y.-M.; Debrunner, P. G.; Chaudhuri, P.; Wieghardt, K. J. Am. Chem. Soc. 1996, 118, 7542-7550.
